An Anglocentric History of Anaesthetics and Analgesics in the Refinement of Animal Experiments - MDPI
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animals
Commentary
An Anglocentric History of Anaesthetics and
Analgesics in the Refinement of Animal Experiments
R. Eddie Clutton
The Wellcome Trust Critical Care Laboratory for Large Animals, Roslin Institute, Easter Bush Veterinary Centre,
Roslin, Midlothian EH25 9RG, UK; e.clutton@ed.ac.uk; Tel.: +44-131-650-6220 or +44-07749-887-342
Received: 14 September 2020; Accepted: 15 October 2020; Published: 21 October 2020
Simple Summary: In simultaneously describing the history of animal experimentation and the
development of anaesthetics and analgesics from an Anglocentric perspective, this article reveals how
the latter have considerably refined animal experiments and brought benefits to both science and
the animals involved—particularly in the 19th and 20th centuries. The more recent development of
training and educational programmes in laboratory animal anaesthesia and their role in maintaining
desirable trends in experimental refinement are also described.
Abstract: Previous histories of animal experimentation, e.g., Franco (2013) have focused on ethics,
the law and the personalities involved, but not on the involvement of anaesthetics or analgesics.
Given that these were major subjects of (UK) Parliamentary debates on vivisection in the mid-19th
century and viewed as “indisputable refinements in animal experimentation” (Russell and Burch
1959), it seemed that an analysis of their role was overdue. This commentary has, in interweaving
the history of animal experimentation in the UK with the evolution of anaesthesia, attempted to: (1)
clarify the evidence for Russell and Burch’s view; and (2) evaluate anaesthesia’s ongoing contribution
to experimental refinement. The history that emerges reveals that the withholding or misuse of
anaesthetics and, or analgesics from laboratory animals in the UK has had a profound effect on
scientists and indirectly on the attitudes of the British public in general, becoming a major driver
for the establishment of the anti-vivisection movement and subsequently, the Cruelty to Animals
Act (1876)—the world’s first legislation for the regulation of animal experimentation. In 1902, the
mismanaged anaesthetic of a dog in the Department of Physiology, University College London
resulted in numerous events of public disorder initiated by medical students against the police and a
political coalition of anti-vivisectionists, trade unionists, socialists, Marxists, liberals and suffragettes.
The importance of anaesthesia in animal experiments was sustained over the following 150 years as
small mammalian species gradually replaced dogs and cats as the principle subjects for vivisection.
In discussing experimental refinement in their 1959 report, “The Principles of Humane Experimental
Technique” Russell and Burch described anaesthetics as “ . . . the greatest single advance in humane
technique, (which) has at the same time been virtually indispensable for the advance of experimental
biology”. Since then, the role of anaesthetics and in particular analgesics has become an unavoidable
consideration whenever animal experiments are planned and conducted. This has been accompanied
by a proliferation of training and educational programmes in laboratory animal anaesthesia.
Keywords: animal research; animal testing; biomedical research; anaesthesia; analgesia; history
of science
1. Introduction
The progression of animal experimentation from classical times to the present has been directed by
the rarely compatible views of “scientists”, philosophers and legislating authorities and, more recently,
Animals 2020, 10, 1933; doi:10.3390/ani10101933 www.mdpi.com/journal/animalsAnimals 2020, 10, 1933 2 of 22
vested interest and the public have become influential. Arguably, the greatest hostility between those
for and against animal vivisection—based largely on the questions of animal sentience and the scientific
value of noxious animal experiments—was seen in the years between the late 18th and early 19th
centuries, when, co-incidentally, the first influential observations on the anaesthetic properties of gases
were reported. The introduction of general anaesthetics into medical practice in the mid-19th century
greatly facilitated surgery by alleviating the (human) patient’s agonies. At the same time, and for
the same reason, many felt that anaesthetics increased the ethical defensibility of animal experiments.
The similarly opining would also claim that in eliminating the widespread and profound physiological
effects of pain and suffering—an effect which had been recognized for some 2300 years—anaesthetics
improved data value and increased the validity of animal experiments. Some scientists countered this
(and continue to do so) by emphasising that anaesthetics and analgesics can produce similar if not
greater degrees of physiological perturbation than the pain itself, and so should be excluded from
experimental protocols. Fortunately (for animals) Russell and Burch’s “The Principles of Humane
Experimental Technique” (1959) [1] established anaesthesia and analgesia as indisputable refinements
in animal experimentation and which, along with reduction and replacement, pervades all stages of
contemporary animal experimentation in the UK, i.e., from funding application and ethical approval
through to the publication of results. A focused historical examination of the contribution of anaesthesia
and analgesia to the refinement of animal experiments has not previously been attempted. This article
reports an Anglocentric view of the role of anaesthetics, analgesics and anaesthetists in reshaping the
attitudes of scientists, philosophers, the authorities and the public to animal experimentation.
Galen, Vesalius and Paracelsus (330BC-1541)
Beginning with a description of surgical procedures conducted on animals without the use of
anaesthetics, i.e., vivisection, reveals an early concern with its morality and an ongoing conviction that
pain has a disruptive effect on experimental results. Thus, scholars of the Empiric School of Medicine
(330 BCE–ca 400 AD) dismissed the study of physiology by vivisection on the grounds of its cruelty
and clinical irrelevance [2]. Early descriptions also reveal an ambivalence by vivisectors towards
animal suffering and a need to justify its practice. Galen preferred using pigs and goats over apes
because, during brain dissections, the unpleasant expression of the ape discomfited him [3]. Vesalius
recognized the cruelty of vivisection but justified it for what it revealed: his thesis “De humani corporis
fabrica libri septem” (“On the Fabric of the Human Body in Seven Books”) (1543) features a small capital
letter “Q” historiating the dissection of a pregnant bitch. (An historiated initial is an enlarged letter at
the beginning of a paragraph that contains a picture.) Whilst conceding that the animal “is cruciata”,
i.e., is crucified or tortured, “it allowed the demonstration of the unborn puppies struggle to breathe
once the placental blood flow was ended” [4]. In the same publication, an historiated capital “Q”
shows a conscious pig—immobilized with chains—undergoing tracheal surgery for the placement
of a tube allowing periodic lung inflation, the first convincing account of artificial ventilation [5].
That restraining chains were required to immobilize the animal suggests that Vesalius was unaware
that, at this time, Paraclesus was using ether (known as sweet oil of vitriol) to produce analgesia in
chickens (although the first edition of Opera Medico-chemica sive paradoxa (“On the Field of Medicinal
Chemistry or Paradoxes”) which contains an account of this was not published until 1605). In this
thesis, Paracelsus proposed that the sweet oil of vitriol:
“...quiets all suffering without any harm and relieves all pain, and quenches all fevers, and prevents
complications in all disease.” [6]
It is unfortunate for both humans and animals that 300 years were to elapse before both
innovations, i.e., positive pressure lung ventilation and inhalant anaesthetics, were re-introduced into
clinical anaesthetic practice.Animals 2020, 10, 1933 3 of 22
Harvey, Descartes and the Oxford Group (1578–1665)
Had they been contemporaries, Paracelsus’ interest in pain relief might have benefitted William
Harvey’s early studies of “the heart’s motion” in conscious animals whose chest walls had been
surgically removed. Harvey complained that the heart’s action was too fast, a complication which
later prompted him to use “colder animals, such as toads, frogs and serpents . . . ” or “dying dogs and
hogs” [7]. That the excessive heart rate was the inescapable result of undergoing thoracic surgery whilst
conscious was not overlooked: O’Meara (1665) argued that, “ . . . the miserable torture of vivisection
places the body in an unnatural state and that amid the terrible pains of vivisection all the juices are
brought to flow together, thus denying the validity of animal experimentation” [3]. Such concerns
may have puzzled French philosopher and vivisector Renee Descartes who believed that animals,
“When burnt with a hot iron or cut with a knife their writhing and screaming are like the creaking of
a hinge, no more” [8]. This belief emboldened some scientists “with less responsible and reflective
minds” [3] to conduct even more gruesome experiments [1] whilst elsewhere, it had the opposite effect
and promoted consternation—even amongst established vivisectionists. Johann Brunner, Professor of
Medicine at Heidelburg, described the animals he dissected as “the martyrs of the anatomists” [3],
whilst members of the Oxford Group, specifically Christopher Wren, Robert Boyle and Robert Hooke,
not only recognized the cruelty of vivisection and its adverse effects on scientific data, but began
preliminary experiments with intravenous anaesthesia. They also considered the use of opium to
alleviate the suffering of experimental dogs [9]. Writing to Boyle on the 10th November 1664, Hooke,
having that year completed a thoracic dissection and lung inflation study in a dog, complained:
“I shall hardly be induc’d to make any further trials of this kind because of the torture of the creature
but certainly the inquiry would be very noble if we could any way find a way soe to stupify the creature
as that it might not be sensible which I fear there is hardly any opiate will performe”.
The reference to opiate use is important because both Wren and Boyle had been conducting
observational studies on the use of alcoholic opiate concoctions in dogs for the previous 8 years [9].
In The Usefulness of Experimental Philosophy (1663), published one year before Hooke’s regretted
thoracotomy study, Boyle described an experiment performed by Wren, who injected a warm solution
of opium in sack (a sweet white dessert-type wine) into the vein of a dog’s hind leg:
“We had scarce untied the dog..., before the opium began to disclose its narcotick quality; and almost
as soon as he was upon his feet, he began to nod with his head, and faulter and reel in his pace, and
presently after appeared so stupified, that there were wagers offered his life could not be saved”. (The
dog survived).
Perhaps aware that “some narckotic” may have alleviated his animal’s suffering, in 1665 a
remorseful Hooke wrote:
“The microscope enables one to look at nature ‘acting according to her usual course and way,
undisturbed, whereas when we endeavour to pry into her secrets by breaking open the doors upon
her, and dissecting and mangling creatures whilst there is life yet within them, we find her indeed at
work, but put into such disorder by the violence offered that we cannot tell if the results are of any
significance”,
He thus revealed his prescient belief that the extreme physiological responses to painful vivisection
were not representative of the normal state. That, he asserted, was only discernible by non-invasive
means, e.g., microscopy [10].
Davy (1778–1829)
In April 1799, Humphry Davy reported his initial findings concerning the inhalation of nitrous
oxide (N2 O) and then embarked upon a series of animal experiments culminating with the publicationAnimals 2020, 10, 1933 4 of 22
of, “Researches Chemical and Philosophical: Chiefly Concerning Nitrous Oxide and its Respiration”,
in 1800. In this, Davy describes guinea pig experiments and the administration of pure nitrous oxide to
a “stout and healthy cat”.
“after 5 min the pulse was hardly perceptible; he made no motions and appeared wholly senseless.
After 5 min and a quarter he was taken out . . . in 8 or 9 min he was able to walk . . . in half an hour he
was completely recovered”.
He frequently inhaled the gas himself, once whilst suffering severe pain from a wisdom tooth
eruption after which he wrote:
“As nitrous oxide in its extensive operation appears capable of destroying physical pain, it may
probably be used with advantage during surgical operations in which no great effusion of blood takes
place.” [11]
Bentham (1748–1841) and Seturner (1783–1841)
That Davy’s findings remained unadopted in medical practice until 1844 is attributed by Cartwright
(1950) to the callousness and unprecedented brutality of the 18th-century Englishman [11]. Such
callousness may have fuelled a growing philosophical interest in animal suffering, as exemplified by
Bentham’s proposal that animals be treated according to their capacity to suffer. In 1789, he asked:
“The question is not, Can they reason? nor, Can they talk? but, Can they suffer?” [12]
Paradoxically, Bentham’s utilitarianism necessitated his support of “justifiable” vivisection. In a
letter to the editor of the Morning Chronicle, 4th March 1825, he wrote:
“Sir—I never have seen, nor ever can see, any objection to the putting of dogs and other inferior
animals to pain, in the way of medical experiment, when that experiment has a determinate object,
beneficial to mankind, accompanied with a fair prospect of the accomplishment of it. But I have a
decided and insuperable objection to the putting of them to pain without any such view”.
While human beings had been capitalising on the analgesic effects of Papaver somniferum derivatives
since prehistory, the use of opioids in animals remained largely unreported until 1805, following
Sertürner’s isolation of morphine [13]. He tested an aqueous alcoholic extraction of the salt on four
dogs and a mouse “that he found wandering in the laboratory”. He gave 6 grains to a dog, followed an
hour later by another 6 grains. The dogs vomited, had convulsions, and were sleepy, but did not sleep.
One “gentle little dog” died. He reported the results of his animal studies in the Journalder Pharmacie
fuer Aerzte und Apotheker in 1806, a reading of which would probably not have convinced anyone of the
new compound’s analgesic potential.
Magendie (1783–1855)
Francoise Magendie was to become the most influential vivisectionist of all time although when
he first began dissecting conscious animals is unknown. Elliott (1987) puts it within a few years of his
first publication (1809) because the essay did not describe vivisection, only an intent to conduct it [14].
By the time of his death in 1855, Magendie had been dubbed the “father of experimental physiology”
and had done more to foment anti-vivisectionist sentiment in the UK than any other “scientist” in
Europe [15]. Descriptions of his vivisections, often performed publicly, abound and reveal absolute
indifference to animal suffering and to those who judged his actions cruel. Admittedly, there was
a lack of effective anaesthesia—at least for the first forty years of his career—but not the final nine
(see Figure 1 for the approximate dates when anaesthetics and analgesics became available for use in
animal experiments). France’s first successful ether anaesthetic was administered on 22 December
1846, with reports on its general and obstetrical use being published in January and February 1847,
respectively [16]. Magendie himself examined the effects of rectal ether and morphine in dogs [17].Animals 2020, 10, x 5 of 24
administered on 22 December 1846, with reports on its general and obstetrical use being published
Animals 2020, 10, 1933 5 of 22
in January and February 1847, respectively [16]. Magendie himself examined the effects of rectal ether
and morphine in dogs [17]. Furthermore, as the first Professor of Physiology at the College de France
and Vice-President
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Magendie rejoined that if his experiments did not serve humanity, they would indeed be cruel.
Magendie rejoined that if his experiments did not serve humanity, they would indeed be cruel.
However, to use animals in order to make discoveries useful to medicine did not merit such reproach
However, to use animals in order to make discoveries useful to medicine did not merit such reproach [18].
[18]. This position applied to anaesthetics. As early as 1847, Magendie had observed that “intoxication
This position applied to anaesthetics. As early as 1847, Magendie had observed that “intoxication
caused by sulphuric ether was “little understood” and that only when it was thoroughly understood
caused by sulphuric ether was “little understood” and that only when it was thoroughly understood
could one safely and with a clear conscience apply it to man” [19].
could one safely and with a clear conscience apply it to man” [19].
Dates of
Figure1.1. Dates
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1986: The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research:
epoc. A(SP)A 1986: The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research: Reporting in Vivo
Experiments; Reporting guidelines. Additional dates for reference: [1]: 1873 Sanderson
Reporting in Vivo Experiments; Reporting guidelines. Additional dates for reference: [1]: 1873 publishes,
“Handbook
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the Physiological Magnan “affair”;
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Hickman (1800–1830)
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objective of inducing reversible unconsciousness in order to facilitate surgery [20].
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puppy was enclosed beneath a glass cover (bell jar) andand
“in ten Minutes he showed great marks of uneasiness, in 12 respiration became difficult, and in
17 Minutes ceased altogether, at 18 Minutes I took off one of the ears, which was not followed byAnimals 2020, 10, 1933 6 of 22
haemorrhage, respiration soon returned and the animal did not appear to be the least sensible to pain,
in three days the ear was perfectly healed” [21]
Hickman’s subsequent pamphlet entitled: “A letter on Suspended Animation containing
experiments showing that it may safely be employed during operations on animals with the view of
ascertaining its probable utility in surgical operations on the Human Subject,” was ignored by the
Royal Society probably because Hickman’s chosen sponsor lacked the necessary enthusiasm for its
fair promotion. Furthermore, an 1826 article in The Lancet authored by “Antiquack” (purportedly a
professionally envious Davy) entitled ‘Surgical Humbug’ ruthlessly criticized his work and prompted
his defection to France, where, despite the support of Napoleon‘s field surgeon, he met a similar
response. Since his premature death in 1830, this and previous failures to recognize the potential of his
work have been the subject of anguished review [22] because it meant Hickman’s prescient desire to
develop surgical anaesthesia in humans took another 20 years for others to achieve.
Martin (1754–1834)
Richard Martin MP in conjunction with Edinburgh-born Lord Erskine succeeded in getting the
“Cruel Treatment of Cattle Act 1822” or ‘Martin’s Act’, passed into British law—the first legislation
against animal cruelty introduced by means of a Parliamentary procedure anywhere in the world.
It received Royal assent on the 22 July 1822. Martin’s Act sought to prevent the cruel and improper
treatment of horses, mares, geldings, mules, asses, cows, heifers, steers, oxen, sheep and other cattle.
The introduction of this and subsequent legislation is shown in Figure 2 (legislation).
Two years later, on 16 June 1824, a meeting was called in Old Slaughters Coffee House, Martins
Lane, London at which various clergymen and anti-slavery campaigners launched the Society for
the Prevention of Cruelty to Animals (SPCA). Martin was also present and tasked to investigate the
markets and streets of the Metropolis, slaughterhouses and the behaviour of coachmen. In 1840,
Victoria I granted the “Royal” prefix, and so the RSPCA was born. Neither Act nor Royal Society were
initially motivated to control animal vivisection although this was soon to change. The foundation of
this and other organisations concerned with vivisection is shown in Figure 2.Animals 2020, 10, 1933 7 of 22
Animals 2020, 10, x FOR PEER REVIEW 7 of 24
FigureFigure
2. Key2. Key events in animal experimentation in the UK partitioned into the introduction of legislative and optional (recommended) constraints, and the formation
events in animal experimentation in the UK partitioned into the introduction of legislative and optional (recommended) constraints, and the formation
of societies that have influenced the use of anaesthetics and analgesics in animal experiments. Alternatively shaded x axis blocks each represent a 50 year epoc.
of societies that have influenced the use of anaesthetics and analgesics in animal experiments. Alternatively shaded x axis blocks each represent a 50 year epoc. A(SP)A
A(SP)A 1986: The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research: Reporting in Vivo Experiments; Reporting guidelines. Additional dates
1986: The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research: Reporting in Vivo Experiments; Reporting guidelines. Additional dates for
for reference: [1]: 1873 Sanderson publishes, “Handbook for the Physiological Laboratory”; [2]: the Magnan “affair”; [3]: the brown dog affair. ALF: Animal
reference: [1]: 1873 Sanderson publishes, “Handbook for the Physiological Laboratory”; [2]: the Magnan “affair”; [3]: the brown dog affair. ALF: Animal Liberation
Liberation Front; AVA: Association of Veterinary Anaesthetists; BAAS: British Association for the Advancement of Science; BLAVA: British Laboratory Animal
Front;Veterinary
AVA: Association of Veterinary Anaesthetists; BAAS: British Association for the Advancement of Science; BLAVA: British Laboratory Animal Veterinary
Association; BUAV: British Union of Anti-vivisectionists; ECVAM: European Centre for the Validation of Alternative Methods; FRAME: Fund for the
Association; BUAV:ofBritish
Replacement AnimalsUnion of Anti-vivisectionists;
in Medical Experiments; IAT:ECVAM:
InstituteEuropean
of AnimalCentre for theLASA:
Technology; Validation of Alternative
Laboratory Methods;
Animal Science FRAME: Fund
Association; NAVS:for the Replacement
National Anti- of
Animals in Medical Experiments; IAT: Institute of Animal Technology; LASA: Laboratory Animal Science Association; NAVS: National Anti-Vivisection Society;
NC3Rs: National Centre for the 3Rs; LAVA: Laboratory Animal Veterinary Association; RDS: Research Defence Society; SPCA: Society for the Prevention of Cruelty to
Animals; UFAW: Universities Federation for Animal Welfare; UAR: Understanding Animal Research.Animals 2020, 10, 1933 8 of 22
Hall (1790–1857)
Marshall Hall, an English neurophysiologist and contemporary of Magendie, pioneered animal
welfare from within science. In 1831, he proposed that physiologic procedures be regulated in a way
that took into consideration the suffering of animals [19]. He called for the formation of a society for
physiological research, which would regulate animal experimentation, for he said, “every experiment
. . . is necessarily attended by pain or suffering of a bodily or mental kind”. In 1835, in his “Principles of
Investigation in Physiology,” he outlined five principles to govern animal experimentation, the fourth
of which stated (in the days before anaesthesia) that “justifiable experiments should be carried out with
the least possible infliction of suffering, often through the use of lower, less sentient animals, such as
frogs and fish or even newly dead animals”. (The other points were that: (1) an experiment should
never be performed if the necessary information could be obtained by observation; (2) no experiment
should be performed without a clearly defined and obtainable objective; (3) scientists should be
well-informed about the work of their predecessors and peers to avoid unnecessary experimental
repetition; (4) vide supra; and (5) every experiment should be performed under circumstances that
would provide the clearest possible results, thereby diminishing the need for repetition of experiments.)
Morton (1819–1868), Glover (1815–1859), Simpson (1811–1870) and Snow (1813–1858)
The birth of medical anaesthesia based upon N2 O and ether in the United States did not depend
on animal experimentation, although Morton tested ether on animals [23] and then patients, before
administering a convincing anaesthetic at the Massachusetts General Hospital on 16 October 1846.
In the UK, Simpson’s eventual “discovery” and promotion of chloroform in 1847 [24] relied
as much on what could be remembered after self-administration as it did upon his own animal
studies. That said, Simpson’s pioneering had been eased by others establishing the compound’s
pharmacological properties through animal testing—namely Robert Glover, whose studies of bromine,
iodine and chlorine compounds, including chloroform and dichlorethane culminated in a thesis entitled
‘On the Physiological and Medicinal Properties of Bromine and its Compounds’. Published in 1842,
this was the first to describe chloroform’s anaesthetic effects. Among various experiments, Glover
injected 30 and 60 minims (1.6 and 3.6 mL) of chloroform into the jugular vein of two dogs, causing
immediate unconsciousness, loss of the eyelid reflex, insensitivity of the paws to painful stimuli and
marked motor weakness, a state from which the dogs quickly recovered. Glover did not test chloroform
by inhalation, although he described its smell on his animals’ breath [25].
Despite Simpson’s inclination to test newly discovered halogenated organic molecules on himself,
it is probable that animal testing saved his life. Having recently synthesized ethylene dibromide,
Wemyss Reid (the Professor of Chemistry at the University of Edinburgh) suggested to Simpson that
it should be tested on rabbits first. Simpson had intended to inhale ethylene dibromide himself but
surrendered the opportunity on discovering the two rabbits so treated had died overnight. It was
subsequently discovered that the inhalation of ethylene dibromide causes pulmonary congestion; it is
currently used as a soil fumigant to kill nematode worms [26].
John Snow—Simpson’s Yorkshire-born contemporary—was described by Waters (1936) as “the first
anaesthetist” because his research spanned basic science and clinical medicine and he answered
fundamental questions with respect to anaesthetic safety [27]. Snow also recognised the importance of
accuracy in anaesthetic delivery and patient monitoring. Investigating ether (and later chloroform),
Snow performed numerous studies on animals, including birds and fish, in which his renowned
attention to detail—at least on one occasion—lapsed. Whilst demonstrating ether anaesthesia on a
thrush to an audience of Military Surgeons, he became distracted and killed the bird [28]. Snow’s
published description of the event reveals the legitimacy of Waters’ accolade.
“This thrush was only in the vapour for about a minute, and it is dead. It had ceased to breathe before
I took it out of the jar. It is a result I did not intend, and it has arisen from my going on with the
lecture, and looking at my notes, instead of directing my whole attention to the animal”.Animals 2020, 10, 1933 9 of 22
Wakley (1795–1862)
On the 19th March 1847, The Times reported the death of Ann Parkinson two days after ether
administration [29]. Chloroform’s first UK victim was Hannah Greener, who died during induction
on 28th January 1848. To assuage growing public concern with the safety of anaesthetics, large-scale
animal studies were conducted [30]. In 1848, Wakley reported a study comparing the effects of ether
and chloroform on 100 animals—predominantly dogs, but also cats, rabbits, rats, mice, guinea pigs,
a hedgehog, a pig, two sheep, a donkey, two mares and some pigeons. From the findings that death
resulted in 11 out of 32 animals (34%) anaesthetized with ether and 30 out of 67 animals (44%) receiving
chloroform, Wakley concluded:
“ . . . assuredly the more dangerous one of the two would be found in the vapour of chloroform”. [31]
However, Youngson (1979) emphasized the studies’ hopelessly unscientific character [22], e.g.,
of the 18 dogs studied, only one received ether (and of the 17 dogs given chloroform, only 4 died (24%)).
Whilst Wakley’s conclusions were based on unsound data, they were nevertheless to prove correct.
Bernard (1813–1878)
Claude Bernard, the “father of modern experimental medicine”, died a revered scientist.
His attitude to the use of animals and anaesthetics in physiological research was influenced by
Magendie under whom he studied from 1834 to 1843. Unlike Magendie, Bernard could not claim
ignorance to justify the exclusion of anaesthetics from most—but not all—of his animal studies [19];
nor could he claim adherence to the vitalist principle which he described as being, “entirely contrary
to science itself”. Bernard’s considerable contributions to anaesthesia [32] were anthropocentric and
achieved at cost to the animals involved. He studied vasomotion—the nervous control of blood vessel
diameter—by cutting projections from the stellate ganglion in unanaesthetized rabbits (so discovering
cervical sympathetic block and its effects on the eye). His most influential and controversial work—on
curare—began in 1844. (Curare is a drug derived from tree bark and applied to blow-dart tips used by
South American Indians to paralyse and capture animals. Curare prevents muscle contraction and
stops all movement, including breathing. However, it does not affect the central nervous system and so
darted animals suffocate whilst being fully conscious. If breathing is artificially supported, a curarised
animal can be subjected to surgery and, although fully aware of the process, is unable to move—or
vocalize—in agonized protestation.) Having demonstrated its neuromuscular blocking effect in frogs,
he used it in dogs to control strychnine-induced convulsions. After further ranine studies, Bernard
suspected that death following curare was caused by asphyxia and not loss of consciousness [33].
The realisation that it did not render the animal insentient prompted him to reflect:
“in the animals, one can judge sensitivity only by motor manifestations. Man alone, on recovering
from poisoning by curare, would be able to say, supposing that he had retained the memory, whether
or not he had suffered”.
He wrote eloquently, and more than once, on his impression of death following
curare administration:
“Within the motionless body, behind the staring eye, with all the appearance of death, feeling and
intelligence persist in all their force. Can we conceive of a suffering more horrible than that of
intelligence present, after succumbing, one by one, of all the organs which are destined to find
themselves imprisoned alive within a cadaver?”
This concern did not prevent Bernard from continuing to use curare rather than anaesthetics in
his experiments. Furthermore, he promoted its use in experiments to other physiologists. An 1864
essay asserts that the ‘poison becomes an instrument which dissociates and analyses the most delicate
phenomena of the living machine’ [34]. Consequently, vivisectors discovered that used in the right
quantities, curare made invasive procedures much easier and the drug became a common experimental
tool in physiological practice.Animals 2020, 10, 1933 10 of 22
Alfort (1846–1863)
For some 17 years, complaints and petitions had been made to various French authorities about the
vivisection of horses at the Veterinary College at Alfort, Paris. The Times of 8 August 1863 reported that,
“ . . . at Alfort a wretched horse is periodically given up to a group of students to experimentalize
upon. They tie him down and torture him for hours, the operations being graduated in such a manner
that sixty and even more may be performed before death ensues”.
British Veterinary Surgeons joined elements of the French Press to demand reform. The attack of
the British Medical Journal was based on the exclusion of anaesthetics:
“It has never appeared clear to us that we are justified in destroying animals for mere experimental
research under any circumstances; but now that we possess the means of removing sensation during
experiments, the man who puts an animal to torture ought, in our opinion, to be prosecuted”
The beneficial role of anaesthetics during noxious animal experiments was being increasingly
recognized. Responding to the Alfort affair, the RSPCA offered a £50 prize for the best essay received on
the subject of vivisection. Dr Markham, Physician to Saint Mary’s Hospital London, and Mr Fleming,
Veterinary Surgeon to the Third Hussars, won prizes for essays recommending the use of anaesthetics
in experiments [15].
Cobbe (1822–1904) and Schiff (1823–1896)
As one of the 19th century’s most effective anti-vivisectionists, the Anglo-Irish reformer Frances
Power Cobbe had a major effect on ensuring anaesthetics became a legal requirement in animal
experiments in the UK. Prompted by the Alfort scandal, she published, “The Rights of Man and the
Claims of Brutes” in 1863. In the same year, she petitioned Moritz Schiff “to spare his animals as much
pain” as possible. In response, Schiff offered that all his animals had anaesthetics. This may have been
true: unlike most of his French and German peers in physiology, Schiff recognized that there
“was a real problem in reconciling the needs of science with the most refined humanitarian sentiment”
and that
“Should the physiologist make use of live animals, he had to suspend their sensitivity, by means of
opium, ether or chloroform, depending on which vital functions he wanted to examine and thus to
maintain as normal” [35]
Burdon-Sanderson (1828–1905) [35]
The concern of other British physiologists with the suffering experimentation caused eventually
prompted the British Association for the Advancement of Science to publish four recommendations in
1871, two of which promoted the use of anaesthetics, i.e.,
(1) No experiment that can be performed under the influence of an anaesthetic ought to be done
without it.
(2) No painful experiment is justifiable for the mere purpose of illustrating a law or fact already
demonstrated; in other words, experimentation without the employment of anaesthetics is not a
fitting exhibition for teaching purposes.
This view was not entirely consensual. In 1873, John Burdon-Sanderson’s Handbook for the
Physiological Laboratory, “a practical description of experimental procedures” was published,
providing Cobbe’s anti-vivisectionists with evidence that scientists were indifferent to animal suffering.
The handbook made no explicit reference to anaesthesia or how and when to use it in experiments.
However, it did index curare, as several contributing authors recommended its use to keep animals
still as an alternative to tying them down. The drug’s inability to affect consciousness had been known
for approximately 20 years.Animals 2020, 10, 1933 11 of 22
Magnan (1847)
Eugene Magnan, another Magendian student, enraged delegates at the 1874 British Medical
Association’s congress by injecting alcohol and absinthe into two dogs. The first animal became “dead
drunk” while the second had an epileptic seizure. Both later died [36]. The event had at least three
consequences. It: (1) made members of the medical profession prosecutable under an amended form of
Martin’s 1822 Act; (2) revealed to both anti-vivisectionists and scientists that a law dealing specifically
with experimental animal protection was required; (3) re-animated Cobbe’s anti-vivisectionism [15].
It also involved an attempted demonstration of intravenous anaesthesia which failed.
Henniker and Playfair (1875)
Cobbe, working with the RSPCA and indirect support from Queen Victoria, lobbied the
Government to legislate against vivisection. In May 1875, the Henniker Bill for Regulating the Practice
of Vivisection was introduced to Parliament [37]. The Bill proposed—amongst other things—that
“recovery (from anaesthesia) experiments required special approval and that anaesthetics be used
in all experiments, excepting those undertaken by individuals with a personal license”. One week
later a second Bill representing the scientists’ views was read. This, the Playfair Bill, proposed the
regulation of painful animal experiments but recommended the legalisation of painless experiments,
including those conducted under anaesthesia. Licenses for painful experiments undertaken without
anaesthesia could be granted on several grounds, including “when the use of anaesthesia interfered
with the experiment”. The two Bills were in unexpected accord over the general undesirability of
painful experiments but sufficiently contradictory to prompt the appointment of a Royal Commission,
the creation of the World’s first anti-vivisection society and the establishment of the Association for the
Advancement of Medicine by Research.
The subsequently appointed Royal Commission of Enquiry spent less time in discussing the
undesirability of painful experiments—over which there was some consensus—than in deliberating
whether curare was an anaesthetic. The final recommendation was that curare would not be considered
an anaesthetic by law, but the rest of the Commission’s findings satisfied neither side who set about
drafting new Bills.
Hoggan (1837–1891)
George Hoggan had worked in Bernard’s laboratory in Paris and published an “extraordinarily
powerful” letter in the London Morning Post on the 2 February1875 describing Bernard’s underuse
of anaesthetics and over-use of curare. He wrote: “We sacrificed daily from one to 3 dogs, besides
rabbits and other animals, and after four years’ experience, I am of the opinion that not one of those
experiments on animals was justified or necessary” [38]. Frustrated with the Commission’s rate of
progress, Cobbe, George Hoggan and others formed the “Victoria Street Society for the Protection of
Animals from Vivisection” on 2 December 1875 [39]. Initially a non-abolitionist society, it aimed to
protect laboratory animals by regulation. Along with the seventh Earl of Shaftesbury, the new society
formulated a second Bill. The Cruelty to Animals Act [40] reached the statute book on 15 August 1876
and required that:
“animals must during the whole of the experiment be under the influence of some anaesthetic of
sufficient power to prevent the animal feeling pain”
and that
“if the pain is likely to continue after the effect of the anaesthetic has ceased, or if any serious injury
has been inflicted on the animal, it be killed before it recovers from the influence of the anaesthetic
which has been administered”;Animals 2020, 10, 1933 12 of 22
Despite the opposition of the scientific lobby, the new Act also clarified that “the substance known
as urari or curare shall not for the purposes of this Act be deemed to be an anaesthetic”.
The Act radicalized the dissatisfied anti-vivisection movement [41]. In 1878, the Victoria Street
Society declared its goal of total abolition of vivisection prompting the resignation of moderates like
George Hoggan. As opposition to vivisection and Victoria Street Society membership grew, the Society
reconfigured and in 1897 became the National Anti-Vivisection Society (NAVS). The following year the
NAVS voted to accept humane animal experimentation in the short-term whilst remaining committed
to a long-term abolitionist goal. Cobbe promptly left to form the British Union for the Abolition of
Vivisection (BUAV) which demanded the total and immediate abolition of animal experiments, which,
as Cruelty Free International, it still does.
Koller (1857–1944) and Corning (1855–1923)
Karl Koller initially tested cocaine hydrochloride to the cornea of rabbits and dogs in 1884 and
reported that, after one-half to one minute, “insensitiveness” was complete and lasted ten minutes [42].
In 1888, Koller moved to the United States and practiced ophthalmic surgery in New York. Here, the
neurologist James Corning injected 20 minims (1.3 mL) of a 2% cocaine solution into the space between
two inferior dorsal vertebrae of a young dog [43]. Within 5 min, he noted incoordination and later,
weakness and anaesthesia of the animal’s hind quarters which resolved completely in approximately 4
h. Local anaesthetic techniques had been discovered.
Hobday (1869–1939)
The veterinary surgeon Sir Frederick Hobday arguably established veterinary anaesthesia as a
specialty for purposes beyond the laboratory. In 1906, he published “Surgical diseases of the dog
and cat: with chapters on anaesthetics and obstetrics”. Chapter 4, entitled, “The administration of
anaesthetics” was 23 pages long, with five pages devoted to local anaesthesia, 16 pages to general
anaesthesia and two pages to morphia and chloral (hydrate) [44]. In 1915, Hobday published the first
book dedicated to the subject, “Anaesthesia & Narcosis of Animals and Birds”. In describing the use of
chloroform, ether, ACE mixture (alcohol, chloroform, ether) ethyl chloride and nitrous oxide for use in
horses, oxen, sheep, goats, pigs, dogs, cats, monkeys, wild and semi-domesticated animals and birds,
Hobday provided information of potential value for improving laboratory animal anaesthesia.
Starling, Bayliss, Dale, Coleridge, Lind-af-Hageby and the brown dog (1902–1910) [45]
Starling (Professor of Physiology at University College London) conducted pancreatic surgery on
a small brown terrier in December 1902. He re-opened the dog’s abdomen in February 1903 before
a class of medical students. On completing the second operation, Starling handed the animal to
Bayliss, who, in making a new wound, contravened the “no re-use” principle extant in the 1876 Act.
During the third operation, the animal “suffered greatly” and made purposeful movements, indicating
inadequate anaesthesia. The dog was finally given to Henry Dale, an unlicensed research student,
who killed the animal. Louise Lind-af-Hageby and Leisa Schartau observed and recorded the events
in, “The Shambles of Science: Extracts from the Diary of Two Students of Physiology”. Stephen Coleridge,
NAVS secretary, read the book and after recognising breaches of the 1876 Act, made a public statement
against Bayliss, who issued a libel suit. Bayliss won the ensuing case but Coleridge won the public:
£5735 was collected and partly paid for a statue of the brown dog which was unveiled in Battersea
Park on 15 September 1906. Medical students vandalized the statue and it became the focus of fighting
between medical pro-vivisectionists, the police, anti-vivisectionists and the locals—who had developed
a fondness for the effigy. The statue’s removal on 10 March 1910 provoked further anger: nine days
later, more than 3000 people marched from Hyde Park Corner to Trafalgar Square, where a public
meeting was held. Politically relevant public unrest had originated from the mismanagement of the
small dog’s anaesthetic.Animals 2020, 10, 1933 13 of 22
Public reaction to the brown dog affair encouraged the appointment of a second Royal Commission
on Vivisection in 1906. Amongst other matters, Stephen Coleridge proposed that the use of curare
should be entirely prohibited in animal experiments. The Commission eventually recommended that
the use of curare in experiments required special certification, that animals in such experiments must
be anaesthetized before the operation and kept anaesthetized until death. They also recommended
that a Home Office appointee should be present during experiments in which curare was used.
Paget (1855–1926) [46]
The publics’ perception of scientists versus anti-vivisectionists began shifting after the brown
dog affair because a link between scientific growth and an improving quality and quantity of life
was becoming apparent. Medical scientists, becoming sensitive to the public’s concerns, were also
making efforts to dispel the accusations of cruelty being made against them whilst capitalising on
the role of animal experimentation in understanding—if not treating—conditions such as diabetes.
This was exemplified by the publication of Stephen Paget’s Experiments on Animals in 1900. A tome
of 381 pages, 24 were devoted to the chapter on “Anæsthetics Used For Animals”—a considerable
improvement from Sanderson’s aforementioned handbook in which advice on anaesthesia was notable
by its absence. Please see Figure 3 for the dates of the publication of material contributing to the
promotion
Animals of xanaesthetics and analgesics in animal experiments.
2020, 10, 15 of 24
Figure 3. Dates of the publication of material contributing to promotion of anaesthetics and analgesics
Figure 3. Dates of the publication of material contributing to promotion of anaesthetics and analgesics
in animal experiments. Alternatively shaded x axis blocks each represent a 50 year epoc. A(SP)A
in animal experiments. Alternatively shaded x axis blocks each represent a 50 year epoc. A(SP)A 1986:
1986: The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research: Reporting in Vivo
The Animals (Scientific Procedures) Act 1986. ARRIVE: Animals in Research: Reporting in Vivo
Experiments; Reporting guidelines. Additional dates for reference: [1]: 1873 Sanderson publishes,
Experiments; Reporting guidelines. Additional dates for reference: [1]: 1873 Sanderson publishes,
“Handbook for the Physiological Laboratory”; [2]: the Magnan “affair”; [3]: the brown dog affair. AVA:
“Handbook for the Physiological Laboratory”; [2]: the Magnan “affair”; [3]: the brown dog affair.
Association of Veterinary Anaesthetists; VAA: Veterinary Anaesthesia and Analgesia. Grindley [47]
AVA: Association of Veterinary Anaesthetists; VAA: Veterinary Anaesthesia and Analgesia. Grindley
Keele and Smith [48] and Chenoweth and Van Dyke [49] are difficult to locate and on 12 September
[47] Keele and Smith [48] and Chenoweth and Van Dyke [49] are difficult to locate and on 12
2020, were unavailable online. Morton and Griffiths [50] is a landmark paper insofar that it was the
September 2020, were unavailable online. Morton and Griffiths [50] is a landmark paper insofar that
first to emphasize an ethical and scientific imperative to use analgesics in laboratory animals.
it was the first to emphasize an ethical and scientific imperative to use analgesics in laboratory
animals.
Wright (1897–1971)
Hobday’s publications were superseded by (J.G.) Wright’s Veterinary Anaesthesia, which was
Wright (1897–1971)
first published in 1942. Its objective was to serve as a student textbook and as a reference manual for
Hobday’s publications were superseded by (J.G.) Wright’s Veterinary Anaesthesia, which was
first published in 1942. Its objective was to serve as a student textbook and as a reference manual for
veterinarians in practice. To this end, the book in all its editions served its purpose well. However,
laboratory animal anaesthesia was never prioritized, e.g., the current (11th edition) edited by Hall
(deceased) Clarke and Trim, covers most of the laboratory animal species albeit subsumed in aAnimals 2020, 10, 1933 14 of 22
veterinarians in practice. To this end, the book in all its editions served its purpose well. However,
laboratory animal anaesthesia was never prioritized, e.g., the current (11th edition) edited by Hall
(deceased) Clarke and Trim, covers most of the laboratory animal species albeit subsumed in a
chapter entitled “Anaesthesia of zoological species (exotic pets, zoo, aquatic, and wild animals)”.
An examination of Figure 3 (below) reveals that the separation of an increasingly specialized laboratory
animal anaesthesia literature from that describing the common domesticated species began with Hall
and Wrights 5th edition (1961).
Hume (1886–1981) Russell (1925–2006) and Burch (1926–1996) [51]
In 1926, Charles Hume founded the University of London Animal Welfare Society which became the
Universities Federation for Animal Welfare (UFAW) in 1938. Its goals “were to ‘tackle animal problems
on a scientific basis, with a maximum of sympathy but a minimum of sentimentality”. Amongst its
formal aims were to enlist the influence of university men and women on behalf of animals, wild and
domestic and to lessen, by methods appropriate to the special character of a university organisation,
the pain and fear inflicted on animals by man. In 1954, Hume appointed William Russell and Rex
Burch and inaugurated a systematic study of the ethical aspects of experimental animal techniques.
Their report, published in 1959 and entitled “The Principles of Humane Experimental Technique”,
condensed humane techniques into three categories; replacement, reduction, and refinement—the 3Rs.
Replacement involved using reliable non-animal methodologies when they existed. When they did
not, reduction meant using the least number of animals to achieve scientific objectives. Refinement
referred to any measure improving the welfare and experiences of animals that could not evade
experimentation by being replaced or surplus to study requirements. In discussing refinement and
anaesthesia Russell and Burch state:
“the most generally important of all is that of anaesthesia, the supreme refinement procedure. This has
occasioned perhaps the greatest single advance in humane technique, and has at the same time been
virtually indispensable for the advance of experimental biology”. [52]
Russell and Burch’s appreciation of anaesthesia can be condensed into four general themes (1) its
importance, arising from its ability to eliminate pain and suffering; (2) concerns with administration,
i.e., doses and timing; (3) the hazards of neuromuscular blocking agents; (4) the promotion of local
anaesthetic techniques.
Croft (1919–2009)
Neither Russell nor Burch were animal anaesthetists and throughout their “Principles” refer—when
necessary—to the experimental work of Phyllis Croft, a veterinary neurologist. For example,
“Croft has also recently (1957) discussed the condition for veterinary and experimental use of the
relaxants or curariform drugs which block neuromuscular transmission among other effects and which
in general should only be used in conjunction with general anaesthesia and in mammals, facilities for
artificial respiration”. [53]
In 1960, Croft, in conjunction with UFAW, published, “An introduction to the anaesthetics of
laboratory animals”. The booklet, which was 31 pages long and written for technicians and junior
graduates who had no previous experience of anaesthesia, described injection technique and the choice
of anaesthetic, and contained sections on practical anaesthesia in rabbits, guinea pigs, hamsters, rats
and mice. The selection of drugs was confined to ether, thiopentone and pentobarbitone, and its
emphasis was on simplicity [54]. Its publication represents the beginnings of a literature devoted to
laboratory animal anaesthesia.Animals 2020, 10, 1933 15 of 22
Littlewood (1965)
By 1963, the number of animals involved in experiments was counted in millions while the
Cruelty to Animals Act (1876) had remained largely unchanged [55]. A Departmental Committee
on Experiments on Animals, chaired by Sir Sidney Littlewood was assigned “to consider the present
control over experiments on living animals, and to consider whether, and if so what, changes are
desirable in the law.” Published in 1965, the Littlewood Report finally established an uncompromising
recognition that, “the use of muscle relaxing drugs which, in effect, renders an animal physically
helpless whilst leaving it fully conscious, opens the way to experiments of extreme cruelty.”
Singer (1974)
Numerous factors, including two world wars, a major economic recession and the fear of nuclear
annihilation distracted public attention from animal experimentation for much of the 20th century.
However, anti-vivisectionism was re-animated in 1974 when “Animal Liberation” was published
by the Australian philosopher Peter Singer. The Animal Liberation Front (ALF), founded in 1976,
considered the work to be the founding philosophical statement of its raison d’etre and subsequently
ensured—through various activities—that the subject of laboratory animal welfare became a matter of
public concern. However, the chapter featuring laboratory animals and entitled “Tools for Research”
tends to overstate the usefulness of in vitro and ex vivo methodologies, while understating the role
of national and institutional controls. It contains harrowing and detailed descriptions of selected
animal experiments, mainly conducted by the US military and psychiatric researchers delivering
noxious agents and, or stimuli to conscious animals—usually primates or dogs. Importantly, the role
of anaesthetics in experimental refinement is poor, or mis-represented. For example, when discussing
the role of animals in traumatic shock research, Singer summarizes scientific consensus with:
“They (the scientists) discouraged the use of anaesthesia . . . the influence of anaesthesia is controversial
. . . and in the reviewer’s opinion prolonged anaesthesia is best avoided.” [56]
and
“Experimenters may consider it unnecessary to include in their reports any mention of what happens
when . . . animals recover consciousness in the midst of an operation because of an improperly
administered anaesthetic . . . ”. [56]
Singer makes no reference to “The Principle of Humane Experimental Technique”, while the
terms “anaesthesia”, “anesthesia” and “analgesia” do not appear in the book’s index. Arguably, a
more balanced analysis of the benefits of anaesthetics and analgesics in animal experiments might
have reduced the number of criminal acts subsequently committed by the ALF against scientists
and their work-places while offsetting the public’s increasing tendency to view scientists as cruel
and uncompassionate.
Holland and Yoxall (1973–1978)
Concerns with unfeeling science may have been allayed had Holland’s 1973 article in the Canadian
Anaesthetists Society Journal [57] been more widely read. Worried about the paucity of information
available for laboratory animal anaesthesia, e.g.,
“ . . . the relatively low standard of veterinary anaesthesia practised, together with the wide variety of
animals which are now being anaesthetized in laboratories and veterinary hospitals”
Holland asserted that:
“vertebrate animals (and perhaps some invertebrates too) have similar pain pathways and similar
perceptions of pain as man—their lack of ability to communicate does not indicate a lack of awareness
of pain and does not condone inhumane treatment”.You can also read
